Functional second harmonic generation microscopy probes molecular dynamics with high temporal resolution

Moritz Förderer; Tihomir Georgiev; Matias Mosqueira; Rainer H. A. Fink; Martin Vogel

doi:10.1364/BOE.7.000525

Functional second harmonic generation microscopy probes molecular dynamics with high temporal resolution

Moritz Förderer, Tihomir Georgiev, Matias Mosqueira, Rainer H. A. Fink, and Martin Vogel

Biomedical Optics Express
Vol. 7,
Issue 2,
pp. 525-541
(2016)
•https://doi.org/10.1364/BOE.7.000525

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Moritz Förderer, Tihomir Georgiev, Matias Mosqueira, Rainer H. A. Fink, and Martin Vogel, "Functional second harmonic generation microscopy probes molecular dynamics with high temporal resolution," Biomed. Opt. Express 7, 525-541 (2016)

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Related Topics
Table of Contents Category
- Microscopy
Optics & Photonics Topics
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The topics in this list come from the OSA Optics and Photonics Topics applied to this article.
Previously assigned OCIS codes
- Functional monitoring and imaging (170.2655)
- Nonlinear microscopy (180.4315)
- Harmonic generation and mixing (190.2620)

About this Article
History
- Original Manuscript: November 18, 2015
- Revised Manuscript: December 18, 2015
- Manuscript Accepted: December 18, 2015
- Published: January 15, 2016

Accessible

Open Access

Abstract

Second harmonic generation (SHG) microscopy is a powerful tool for label free ex vivo or in vivo imaging, widely used to investigate structure and organization of endogenous SHG emitting proteins such as myosin or collagen. Polarization resolved SHG microscopy renders supplementary information and is used to probe different molecular states. This development towards functional SHG microscopy is calling for new methods for high speed functional imaging of dynamic processes. In this work we present two approaches with linear polarized light and demonstrate high speed line scan measurements of the molecular dynamics of the motor protein myosin with a time resolution of 1 ms in mammalian muscle cells. Such a high speed functional SHG microscopy has high potential to deliver new insights into structural and temporal molecular dynamics under ex vivo or in vivo conditions.

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References

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Publication

Y. Guo, P. P. Ho, H. Savage, D. Harris, P. Sacks, S. Schantz, F. Liu, N. Zhadin, and R. R. Alfano, “Second-harmonic tomography of tissues,” Opt. Lett. 22(17), 1323–1325 (1997).
[Crossref] [PubMed]
P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]
M. Both, M. Vogel, R. H. Fink, and D. Uttenweiler, “Second harmonic generation imaging in muscle fibers,” Proc. SPIE 5139, 112–120 (2003).
[Crossref]
M. Both, M. Vogel, O. Friedrich, F. von Wegner, T. Künsting, R. H. Fink, and D. Uttenweiler, “Second harmonic imaging of intrinsic signals in muscle fibers in situ,” J. Biomed. Opt. 9(5), 882–892 (2004).
[Crossref] [PubMed]
S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]
S. Schürmann, F. von Wegner, R. H. Fink, O. Friedrich, and M. Vogel, “Second harmonic generation microscopy probes different states of motor protein interaction in myofibrils,” Biophys. J. 99(6), 1842–1851 (2010).
[Crossref] [PubMed]
S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70(4), 1637–1643 (1979).
[Crossref]
M. E. Llewellyn, R. P. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[PubMed]
S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]
A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups--SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
[Crossref] [PubMed]
W. Liu, N. Raben, and E. Ralston, “Quantitative evaluation of skeletal muscle defects in second harmonic generation images,” J. Biomed. Opt. 18(2), 026005 (2013).
[Crossref] [PubMed]
G. Recher, P. Coumailleau, D. Rouède, and F. Tiaho, “Structural origin of the drastic modification of second harmonic generation intensity pattern occurring in tail muscles of climax stages xenopus tadpoles,” J. Struct. Biol. 190(1), 1–10 (2015).
[Crossref] [PubMed]
E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref] [PubMed]
F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007).
[Crossref] [PubMed]
A. Wingert, H. Seim, S. Schürmann, R. H. A. Fink, and M. Vogel, “Signal Efficiency in Gradient Index Lens Based Two Photon Microscopy,” Open J. Biophys. 3(1), 43–50 (2013).
[Crossref]
T. Boulesteix, E. Beaurepaire, M. P. Sauviat, and M. C. Schanne-Klein, “Second-harmonic microscopy of unstained living cardiac myocytes: measurements of sarcomere length with 20-nm accuracy,” Opt. Lett. 29(17), 2031–2033 (2004).
[Crossref] [PubMed]
S. J. Wallace, J. L. Morrison, K. J. Botting, and T. W. Kee, “Second-harmonic generation and two-photon-excited autofluorescence microscopy of cardiomyocytes: quantification of cell volume and myosin filaments,” J. Biomed. Opt. 13(6), 064018 (2008).
[Crossref] [PubMed]
S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express 17(12), 10168–10176 (2009).
[Crossref] [PubMed]
C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express 16(20), 16151–16165 (2008).
[Crossref] [PubMed]
S. Psilodimitrakopoulos, S. I. Santos, I. Amat-Roldan, A. K. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt. 14(1), 014001 (2009).
[Crossref] [PubMed]
G. Recher, D. Rouède, P. Richard, A. Simon, J. J. Bellanger, and F. Tiaho, “Three distinct sarcomeric patterns of skeletal muscle revealed by SHG and TPEF microscopy,” Opt. Express 17(22), 19763–19777 (2009).
[Crossref] [PubMed]
D. G. Winters, D. R. Smith, P. Schlup, and R. A. Bartels, “Measurement of orientation and susceptibility ratios using a polarization-resolved second-harmonic generation holographic microscope,” Biomed. Opt. Express 3(9), 2004–2011 (2012).
[Crossref] [PubMed]
S. Brasselet, “Polarization-resolved nonlinear microscopy: application to structural molecular and biological imaging,” Adv. Opt. Photonics 3(3), 205–271 (2011).
[Crossref]
N. Mazumder, C. W. Hu, J. Qiu, M. R. Foreman, C. M. Romero, P. Török, and F. J. Kao, “Revealing molecular structure and orientation with Stokes vector resolved second harmonic generation microscopy,” Methods 66(2), 237–245 (2014).
[Crossref] [PubMed]
V. Nucciotti, C. Stringari, L. Sacconi, F. Vanzi, L. Fusi, M. Linari, G. Piazzesi, V. Lombardi, and F. S. Pavone, “Probing myosin structural conformation in vivo by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 107(17), 7763–7768 (2010).
[Crossref] [PubMed]
J. R. Blinks, R. Rüdel, and S. R. Taylor, “Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin,” J. Physiol. 277(1), 291–323 (1978).
[Crossref] [PubMed]
C. H. Lien, K. Tilbury, S. J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in Second Harmonic Generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
[Crossref] [PubMed]
S. Psilodimitrakopoulos, P. Loza-Alvarez, and D. Artigas, “Fast monitoring of in-vivo conformational changes in myosin using single scan polarization-SHG microscopy,” Biomed. Opt. Express 5(12), 4362–4373 (2014).
[Crossref] [PubMed]
D. A. Kleinman, “Nonlinear dielectric polarization in optical media,” Phys. Rev. 126(6), 1977–1979 (1962).
[Crossref]
F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express 15(19), 12286–12295 (2007).
[Crossref] [PubMed]
C. Teulon, I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Theoretical, numerical and experimental study of geometrical parameters that affect anisotropy measurements in polarization-resolved SHG microscopy,” Opt. Express 23(7), 9313–9328 (2015).
[Crossref] [PubMed]
I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[Crossref] [PubMed]
S. Brasselet, D. Aït-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express 18(14), 14859–14870 (2010).
[Crossref] [PubMed]
O. Friedrich, T. Ehmer, and R. H. A. Fink, “Calcium currents during contraction and shortening in enzymatically isolated murine skeletal muscle fibres,” J. Physiol. 517(3), 757–770 (1999).
[Crossref] [PubMed]
A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second harmonic generation and atomic force microscopy,” Langmuir 20(19), 8165–8171 (2004).
[Crossref] [PubMed]
D. Rouède, J. J. Bellanger, J. Bomo, G. Baffet, and F. Tiaho, “Linear least square (LLS) method for pixel-resolution analysis of polarization dependent SHG images of collagen fibrils,” Opt. Express 23(10), 13309–13319 (2015).
[Crossref] [PubMed]
C. K. Chou, W. L. Chen, P. T. Fwu, S. J. Lin, H. S. Lee, and C. Y. Dong, “Polarization ellipticity compensation in polarization second-harmonic generation microscopy without specimen rotation,” J. Biomed. Opt. 13(1), 014005 (2008).
[Crossref] [PubMed]
A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref] [PubMed]

2015 (3)

G. Recher, P. Coumailleau, D. Rouède, and F. Tiaho, “Structural origin of the drastic modification of second harmonic generation intensity pattern occurring in tail muscles of climax stages xenopus tadpoles,” J. Struct. Biol. 190(1), 1–10 (2015).
[Crossref] [PubMed]

C. Teulon, I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Theoretical, numerical and experimental study of geometrical parameters that affect anisotropy measurements in polarization-resolved SHG microscopy,” Opt. Express 23(7), 9313–9328 (2015).
[Crossref] [PubMed]

D. Rouède, J. J. Bellanger, J. Bomo, G. Baffet, and F. Tiaho, “Linear least square (LLS) method for pixel-resolution analysis of polarization dependent SHG images of collagen fibrils,” Opt. Express 23(10), 13309–13319 (2015).
[Crossref] [PubMed]

2014 (2)

S. Psilodimitrakopoulos, P. Loza-Alvarez, and D. Artigas, “Fast monitoring of in-vivo conformational changes in myosin using single scan polarization-SHG microscopy,” Biomed. Opt. Express 5(12), 4362–4373 (2014).
[Crossref] [PubMed]

N. Mazumder, C. W. Hu, J. Qiu, M. R. Foreman, C. M. Romero, P. Török, and F. J. Kao, “Revealing molecular structure and orientation with Stokes vector resolved second harmonic generation microscopy,” Methods 66(2), 237–245 (2014).
[Crossref] [PubMed]

2013 (4)

A. Wingert, H. Seim, S. Schürmann, R. H. A. Fink, and M. Vogel, “Signal Efficiency in Gradient Index Lens Based Two Photon Microscopy,” Open J. Biophys. 3(1), 43–50 (2013).
[Crossref]

A. Buttgereit, C. Weber, C. S. Garbe, and O. Friedrich, “From chaos to split-ups--SHG microscopy reveals a specific remodelling mechanism in ageing dystrophic muscle,” J. Pathol. 229(3), 477–485 (2013).
[Crossref] [PubMed]

W. Liu, N. Raben, and E. Ralston, “Quantitative evaluation of skeletal muscle defects in second harmonic generation images,” J. Biomed. Opt. 18(2), 026005 (2013).
[Crossref] [PubMed]

C. H. Lien, K. Tilbury, S. J. Chen, and P. J. Campagnola, “Precise, motion-free polarization control in Second Harmonic Generation microscopy using a liquid crystal modulator in the infinity space,” Biomed. Opt. Express 4(10), 1991–2002 (2013).
[Crossref] [PubMed]

2012 (2)

A. E. Tuer, M. K. Akens, S. Krouglov, D. Sandkuijl, B. C. Wilson, C. M. Whyne, and V. Barzda, “Hierarchical model of fibrillar collagen organization for interpreting the second-order susceptibility tensors in biological tissue,” Biophys. J. 103(10), 2093–2105 (2012).
[Crossref] [PubMed]

D. G. Winters, D. R. Smith, P. Schlup, and R. A. Bartels, “Measurement of orientation and susceptibility ratios using a polarization-resolved second-harmonic generation holographic microscope,” Biomed. Opt. Express 3(9), 2004–2011 (2012).
[Crossref] [PubMed]

2011 (1)

S. Brasselet, “Polarization-resolved nonlinear microscopy: application to structural molecular and biological imaging,” Adv. Opt. Photonics 3(3), 205–271 (2011).
[Crossref]

2010 (4)

S. Brasselet, D. Aït-Belkacem, A. Gasecka, F. Munhoz, S. Brustlein, and S. Brasselet, “Influence of birefringence on polarization resolved nonlinear microscopy and collagen SHG structural imaging,” Opt. Express 18(14), 14859–14870 (2010).
[Crossref] [PubMed]

I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[Crossref] [PubMed]

V. Nucciotti, C. Stringari, L. Sacconi, F. Vanzi, L. Fusi, M. Linari, G. Piazzesi, V. Lombardi, and F. S. Pavone, “Probing myosin structural conformation in vivo by second-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 107(17), 7763–7768 (2010).
[Crossref] [PubMed]

S. Schürmann, F. von Wegner, R. H. Fink, O. Friedrich, and M. Vogel, “Second harmonic generation microscopy probes different states of motor protein interaction in myofibrils,” Biophys. J. 99(6), 1842–1851 (2010).
[Crossref] [PubMed]

2009 (3)

S. Psilodimitrakopoulos, D. Artigas, G. Soria, I. Amat-Roldan, A. M. Planas, and P. Loza-Alvarez, “Quantitative discrimination between endogenous SHG sources in mammalian tissue, based on their polarization response,” Opt. Express 17(12), 10168–10176 (2009).
[Crossref] [PubMed]

G. Recher, D. Rouède, P. Richard, A. Simon, J. J. Bellanger, and F. Tiaho, “Three distinct sarcomeric patterns of skeletal muscle revealed by SHG and TPEF microscopy,” Opt. Express 17(22), 19763–19777 (2009).
[Crossref] [PubMed]

S. Psilodimitrakopoulos, S. I. Santos, I. Amat-Roldan, A. K. Thayil, D. Artigas, and P. Loza-Alvarez, “In vivo, pixel-resolution mapping of thick filaments’ orientation in nonfibrilar muscle using polarization-sensitive second harmonic generation microscopy,” J. Biomed. Opt. 14(1), 014001 (2009).
[Crossref] [PubMed]

2008 (6)

C. K. Chou, W. L. Chen, P. T. Fwu, S. J. Lin, H. S. Lee, and C. Y. Dong, “Polarization ellipticity compensation in polarization second-harmonic generation microscopy without specimen rotation,” J. Biomed. Opt. 13(1), 014005 (2008).
[Crossref] [PubMed]

C. Odin, T. Guilbert, A. Alkilani, O. P. Boryskina, V. Fleury, and Y. Le Grand, “Collagen and myosin characterization by orientation field second harmonic microscopy,” Opt. Express 16(20), 16151–16165 (2008).
[Crossref] [PubMed]

M. E. Llewellyn, R. P. Barretto, S. L. Delp, and M. J. Schnitzer, “Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans,” Nature 454(7205), 784–788 (2008).
[PubMed]

S. V. Plotnikov, A. M. Kenny, S. J. Walsh, B. Zubrowski, C. Joseph, V. L. Scranton, G. A. Kuchel, D. Dauser, M. Xu, C. C. Pilbeam, D. J. Adams, R. P. Dougherty, P. J. Campagnola, and W. A. Mohler, “Measurement of muscle disease by quantitative second-harmonic generation imaging,” J. Biomed. Opt. 13(4), 044018 (2008).
[Crossref] [PubMed]

S. J. Wallace, J. L. Morrison, K. J. Botting, and T. W. Kee, “Second-harmonic generation and two-photon-excited autofluorescence microscopy of cardiomyocytes: quantification of cell volume and myosin filaments,” J. Biomed. Opt. 13(6), 064018 (2008).
[Crossref] [PubMed]

E. Ralston, B. Swaim, M. Czapiga, W. L. Hwu, Y. H. Chien, M. G. Pittis, B. Bembi, O. Schwartz, P. Plotz, and N. Raben, “Detection and imaging of non-contractile inclusions and sarcomeric anomalies in skeletal muscle by second harmonic generation combined with two-photon excited fluorescence,” J. Struct. Biol. 162(3), 500–508 (2008).
[Crossref] [PubMed]

2007 (2)

F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007).
[Crossref] [PubMed]

F. Tiaho, G. Recher, and D. Rouède, “Estimation of helical angles of myosin and collagen by second harmonic generation imaging microscopy,” Opt. Express 15(19), 12286–12295 (2007).
[Crossref] [PubMed]

2006 (1)

S. V. Plotnikov, A. C. Millard, P. J. Campagnola, and W. A. Mohler, “Characterization of the myosin-based source for second-harmonic generation from muscle sarcomeres,” Biophys. J. 90(2), 693–703 (2006).
[Crossref] [PubMed]

2004 (3)

M. Both, M. Vogel, O. Friedrich, F. von Wegner, T. Künsting, R. H. Fink, and D. Uttenweiler, “Second harmonic imaging of intrinsic signals in muscle fibers in situ,” J. Biomed. Opt. 9(5), 882–892 (2004).
[Crossref] [PubMed]

T. Boulesteix, E. Beaurepaire, M. P. Sauviat, and M. C. Schanne-Klein, “Second-harmonic microscopy of unstained living cardiac myocytes: measurements of sarcomere length with 20-nm accuracy,” Opt. Lett. 29(17), 2031–2033 (2004).
[Crossref] [PubMed]

A. Leray, L. Leroy, Y. Le Grand, C. Odin, A. Renault, V. Vié, D. Rouède, T. Mallegol, O. Mongin, M. H. V. Werts, and M. Blanchard-Desce, “Organization and orientation of amphiphilic push-pull chromophores deposited in Langmuir-Blodgett monolayers studied by second harmonic generation and atomic force microscopy,” Langmuir 20(19), 8165–8171 (2004).
[Crossref] [PubMed]

2003 (1)

M. Both, M. Vogel, R. H. Fink, and D. Uttenweiler, “Second harmonic generation imaging in muscle fibers,” Proc. SPIE 5139, 112–120 (2003).
[Crossref]

2002 (1)

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, “Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues,” Biophys. J. 82(1), 493–508 (2002).
[Crossref] [PubMed]

1999 (1)

O. Friedrich, T. Ehmer, and R. H. A. Fink, “Calcium currents during contraction and shortening in enzymatically isolated murine skeletal muscle fibres,” J. Physiol. 517(3), 757–770 (1999).
[Crossref] [PubMed]

1997 (1)

Y. Guo, P. P. Ho, H. Savage, D. Harris, P. Sacks, S. Schantz, F. Liu, N. Zhadin, and R. R. Alfano, “Second-harmonic tomography of tissues,” Opt. Lett. 22(17), 1323–1325 (1997).
[Crossref] [PubMed]

1979 (1)

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70(4), 1637–1643 (1979).
[Crossref]

1978 (1)

J. R. Blinks, R. Rüdel, and S. R. Taylor, “Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin,” J. Physiol. 277(1), 291–323 (1978).
[Crossref] [PubMed]

1962 (1)

D. A. Kleinman, “Nonlinear dielectric polarization in optical media,” Phys. Rev. 126(6), 1977–1979 (1962).
[Crossref]

Adams, D. J.

Aït-Belkacem, D.

Akens, M. K.

Alfano, R. R.

Alkilani, A.

Amat-Roldan, I.

Artigas, D.

Baffet, G.

Barretto, R. P.

Bartels, R. A.

Barzda, V.

Beaurepaire, E.

Bellanger, J. J.

Bembi, B.

Blanchard-Desce, M.

Blinks, J. R.

J. R. Blinks, R. Rüdel, and S. R. Taylor, “Calcium transients in isolated amphibian skeletal muscle fibres: detection with aequorin,” J. Physiol. 277(1), 291–323 (1978).
[Crossref] [PubMed]

Bomo, J.

Boryskina, O. P.

Both, M.

M. Both, M. Vogel, R. H. Fink, and D. Uttenweiler, “Second harmonic generation imaging in muscle fibers,” Proc. SPIE 5139, 112–120 (2003).
[Crossref]

Botting, K. J.

Boulesteix, T.

Brasselet, S.

S. Brasselet, “Polarization-resolved nonlinear microscopy: application to structural molecular and biological imaging,” Adv. Opt. Photonics 3(3), 205–271 (2011).
[Crossref]

Brustlein, S.

Buttgereit, A.

Campagnola, P. J.

Chen, S. J.

Chen, W. L.

Chien, Y. H.

Chou, C. K.

Coumailleau, P.

Czapiga, M.

Dauser, D.

Delp, S. L.

Dong, C. Y.

Dougherty, R. P.

Ehmer, T.

Fink, R. H.

M. Both, M. Vogel, R. H. Fink, and D. Uttenweiler, “Second harmonic generation imaging in muscle fibers,” Proc. SPIE 5139, 112–120 (2003).
[Crossref]

Fink, R. H. A.

A. Wingert, H. Seim, S. Schürmann, R. H. A. Fink, and M. Vogel, “Signal Efficiency in Gradient Index Lens Based Two Photon Microscopy,” Open J. Biophys. 3(1), 43–50 (2013).
[Crossref]

Fleury, V.

Foreman, M. R.

Freund, I.

S. Roth and I. Freund, “Second harmonic generation in collagen,” J. Chem. Phys. 70(4), 1637–1643 (1979).
[Crossref]

Friedrich, O.

Fusi, L.

Fwu, P. T.

Garbe, C. S.

Gasecka, A.

Guilbert, T.

Guo, Y.

Gusachenko, I.

I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[Crossref] [PubMed]

Harris, D.

Ho, P. P.

Hoppe, P. E.

Hu, C. W.

Hwu, W. L.

Joseph, C.

Kao, F. J.

Kee, T. W.

Kenny, A. M.

Kleinman, D. A.

D. A. Kleinman, “Nonlinear dielectric polarization in optical media,” Phys. Rev. 126(6), 1977–1979 (1962).
[Crossref]

Krouglov, S.

Kuchel, G. A.

Künsting, T.

Latour, G.

I. Gusachenko, G. Latour, and M. C. Schanne-Klein, “Polarization-resolved Second Harmonic microscopy in anisotropic thick tissues,” Opt. Express 18(18), 19339–19352 (2010).
[Crossref] [PubMed]

Le Grand, Y.

Lee, H. S.

Légaré, F.

F. Légaré, C. Pfeffer, and B. R. Olsen, “The role of backscattering in SHG tissue imaging,” Biophys. J. 93(4), 1312–1320 (2007).
[Crossref] [PubMed]

Leray, A.

Leroy, L.

Lien, C. H.

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Fig. 1 (A) Setup configuration prepared to detect the Ix and Iy components of the SHG signal. (B) Sample image of the Ix SHG signal generated in a skinned EDL fiber bundle in relaxed state with a sample ROI (marked in yellow). (C) Sample image of the Iy SHG signal generated in a resting intact IO fiber with a sample ROI. For visualization purposes, pixels with very large gray values are displayed in white (occurrence <0.01% of total number of pixels).

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Fig. 2 Measurement results gathered with method #1. (A) Relative change of the tensor components χ(xxx) (blue) and χ(xyy) (green) following a conformational change in EDL fiber bundles from rigor to relaxed state. Mean values of the ratios were 2.3 ± 0.4 (mean ± standard deviation) for the χ(xxx) and 1.5 ± 0.2 for the χ(xyy) tensor component (see Eq. (4), the rigor state is defined as S2). (B) Control values of γ for relaxed (black dots) and rigor state (red dots) of the same ROIs calculated with Eq. (8).

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Fig. 3 Measurement results gathered with method #2 (single angle polarimetric approach) at a polarization angle of 18°. (A) Parameter γ on EDL fiber bundles in relaxed and rigor state. Results were 0.45 ± 0.08 (mean ± standard deviation) for relaxed state (black line) and 0.70 ± 0.08 for rigor state (red line), respectively. (B) Control values for γ: 0.45 ± 0.04 for relaxed state, 0.75 ± 0.06 for rigor state.

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Fig. 4 Analysis of the impact of sideways shifts of the sample on the parameter γ in resting IO fibers with method #2 for angular errors of −10° to + 10°: the polarization angle and the PBS were simultaneously turned from + 10 to −10°. (A) Mean values and standard deviations of parameter γ at different angular errors of the sample (black) and the modeled values γ* (red) calculated with Eq. (7) assuming an inaccuracy of −1.5° for the polarization angle and −2° for the PBS and using the γ(0°) value of the experimental data. Ix and Iy were calculated with Eq. (2) by setting Bχ²(xyy) = 1. (B) Relative deviation of γ from γ(0°). (C) Mean values and standard deviations of the Ix and Iy signal. (D) Normalized values of the model for (Ix)* and (Iy)* corresponding to the modeled values in panel A.

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Fig. 5 Series of high speed line scans of an electrically stimulated IO fiber embedded in 5% low melting agarose at increasing voltages (see panels A, B, C, D) and 0.5 ms pulse duration: (A) 16V with the raw line scans for Ix and Iy (29.76µm x 512 ms), the differential γ signal (dγ, black) and differential calcium signal (dCa, red) and the Ix (blue) and Iy (green) signals. (B) Differential signals of γ and calcium for 20 V. (C) Differential signals of γ and calcium for 24 V. (D) Same as A for 28 V. dγ and Ix, Iy values were processed with a 5 point moving-window-average in all panels. For visualization purposes pixels with large gray values are displayed in white in the images (occurrence <0.1% of total number of pixels).

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Fig. 6 Theoretical estimation of the impact of an axial misalignment of the sample on the γ value with a simplified model assuming an oblique incident laser beam.

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Fig. 7 Examples of moving artifacts during contraction measured on an electrically stimulated IO fiber that was not embedded in agarose. γ signal, polarization components signals, calcium signal and Iy line scan images (29.76 µm x 512 ms) are displayed. (A) Movement to the negative direction. (B) Movement to the positive direction. γ, Ix and Iy were processed with a 5 point moving-window-average. For visualization purposes pixels with large gray values are displayed in white in the images (occurrence <0.1% of total number of pixels).

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Tables (1)

Table 1 Comparison of control values to the γ values (mean ± standard deviation) of resting IO fibers measured with method #2 for different polarization angles. In addition to ROIs with myosin bands perpendicular to the scan direction (denoted as “exact ROI”) ROIs with inclined bands were analyzed (denoted as “inclined ROI”).

View Table

Equations (14)

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P_{i} = \sum_{j k} χ_{i j k} E_{j} E_{k},

\begin{array}{l} I_{x} (α) = B χ_{x y y}^{2} {[γ \cos^{2} (α) + \sin^{2} (α)]}^{2}, \\ I_{y} (α) = B χ_{x y y}^{2} {[\sin (2 α)]}^{2}, \end{array}

γ = \frac{χ_{x x x}}{χ_{x y y}} .

\begin{array}{l} \frac{χ_{x x x}^{(S 2)}}{χ_{x x x}^{(S 1)}} = \sqrt{\frac{I^{(S 2)} (0 °)}{I^{(S 1)} (0 °)}}, \\ \frac{χ_{x y y}^{(S 2)}}{χ_{x y y}^{(S 1)}} = \sqrt{\frac{I^{(S 2)} (90 °)}{I^{(S 1)} (90 °)}} . \end{array}

\frac{γ^{(S 2)}}{γ^{(S 1)}} = (\frac{χ_{x x x}^{(S 2)}}{χ_{x x x}^{(S 1)}}) / (\frac{χ_{x y y}^{(S 2)}}{χ_{x y y}^{(S 1)}}) .

γ = \tan (α) [2 \sqrt{\frac{I_{x} (α)}{I_{y} (α)}} - \tan (α)] .

γ^{*} = \tan (α) [2 \sqrt{\frac{I_{x}^{*}}{I_{y}^{*}}} - \tan (α)],

\frac{I_{x}^{*}}{I_{y}^{*}} = \frac{I_{x}^{} \cos^{2} (Δ β - Δ φ) + I_{y}^{} \sin^{2} (Δ β - Δ φ) + \sin (2 (Δ β - Δ φ)) \sqrt{I_{x}^{} I_{y}^{}}}{I_{x}^{} \sin^{2} (Δ β - Δ φ) + I_{y}^{} \cos^{2} (Δ β - Δ φ) - \sin (2 (Δ β - Δ φ)) \sqrt{I_{x}^{} I_{y}^{}}},

\begin{array}{l} I_{x} = I_{x} (α + Δ α - Δ φ), \\ I_{y} = I_{y} (α + Δ α - Δ φ) . \end{array}

γ = \sqrt{\frac{I (0 °)}{I (90 °)}},

\begin{array}{l} I^{*} (0 °, Δ ξ) = B χ_{x y y}^{2} [(^{γ \cos^{2} (Δ ξ) + \sin^{2} (Δ ξ)) 2} + \sin^{2} (2 Δ ξ)], \\ I^{*} (90 °, Δ ξ) = B χ_{x y y}^{2} . \end{array}

\begin{array}{l} χ_{x x x} = N_{S} β_{e} \cos ³ θ_{e}, \\ χ_{x y y} = \frac{1}{2} N_{S} β_{e} \cos θ_{e} \sin ² θ_{e} . \end{array}

γ = \frac{2}{\tan ² θ_{e}} .

\begin{array}{l} \frac{β_{e}^{(S 2)}}{β_{e}^{(S 1)}} = \frac{χ_{x x x}^{(S 2)}}{χ_{x x x}^{(S 1)}} \frac{\cos ³ θ_{e}^{(S 1)}}{\cos ³ θ_{e}^{(S 2)}}, \\ \frac{β_{e}^{(S 2)}}{β_{e}^{(S 1)}} = \frac{χ_{x y y}^{(S 2)}}{χ_{x y y}^{(S 1)}} \frac{\cos θ_{e}^{(S 1)} \sin ² θ_{e}^{(S 1)}}{\cos θ_{e}^{(S 2)} \sin ² θ_{e}^{(S 2)}} . \end{array}

	Control	18° polarization	40° polarization	60° polarization
Exact ROI	0.61 ± 0.04	0.62 ± 0.05	0.63 ± 0.11	0.58 ± 0.36
Inclined ROI	0.62 ± 0.07	0.63 ± 0.11	0.70 ± 0.15	0.97 ± 0.60